Publications

Publications in peer reviewed journals

13 Publications found
  • Beta diversity and oligarchic dominance in the tropical forests of Southern Costa Rica

    Morera-Beita A, Sánchez D, Wanek W, Hofhansl F, Huber W, Chacón-Madrigal E, Montero-Munoz JL, Silla F
    2019 - Biotropica, 51: 117-128

    Abstract: 

    Recent studies have reported a consistent pattern of strong dominance of a small subset of tree species in neotropical forests. These species have been called “hyperdominant” at large geographical scales and “oligarchs” at regional‐landscape scales when being abundant and frequent. Forest community assembly is shaped by environmental factors and stochastic processes, but so far the contribution of oligarchic species to the variation of community composition (i.e., beta diversity) remains poorly known. To that end, we established 20.1‐ha plots, that is, five sites with four forest types (ridge, slope and ravine primary forest, and secondary forest) per site, in humid lowland tropical forests of southwestern Costa Rica to (a) investigate how community composition responds to differences in topography, successional stage, and distance among plots for different groups of species (all, oligarch, common and rare/very rare species) and (b) identify oligarch species characterizing changes in community composition among forest types. From a total of 485 species of trees, lianas and palms recorded in this study only 27 species (i.e., 6%) were nominated as oligarch species. Oligarch species accounted for 37% of all recorded individuals and were present in at least half of the plots. Plant community composition significantly differed among forest types, thus contributing to beta diversity at the landscape scale. Oligarch species was the component best explained by geographical and topographic variables, allowing a confident characterization of the beta diversity among tropical lowland forest stands.

  • Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli

    2019 - Frontiers in Plant Science, 10: Article 157

    Abstract: 

    Root exudation is an important process determining plant interactions with the soil environment. Many studies have linked this process to soil nutrient mobilization. Yet, it remains unresolved how exudation is controlled and how exactly and under what circumstances plants benefit from exudation. The majority of root exudates include primary metabolites (sugars, amino acids and organic acids) believed to be passively lost from the root and used by rhizosphere-dwelling microbes. In this review, we synthetize recent advances in ecology and plant biology to explain and propose mechanisms by which root exudation of primary metabolites is controlled, and what role their exudation plays in plant nutrient acquisition strategies. Specifically, we propose a novel conceptual framework for root exudates. This framework is built upon two main concepts: (i) root exudation of primary metabolites is driven by diffusion, with plants and microbes both modulating concentration gradients and therefore diffusion rates to soil depending on their nutritional status; (ii) exuded metabolite concentrations can be sensed at the root tip and signals are translated to modify root architecture. The flux of primary metabolites through root exudation is mostly located at the root tip, where the lack of cell differentiation favors diffusion of metabolites to the soil. We show examples of how the root tip senses concentration changes of exuded metabolites and translate that into signals to modify root growth. Plants can modify the concentration of metabolites either by controlling source/sink processes or by expressing and regulating efflux carriers, therefore challenging the idea of root exudation as a purely unregulated passive process. Through root exudate flux, plants can locally enhance concentrations of many common metabolites which can serve as sensors and integrators of the plant nutritional status and of the nutrient availability in the surrounding environment. Plant-associated micro-organisms also constitute a strong sink for plant carbon thereby increasing concentration gradients of metabolites and affecting root exudation. Understanding the mechanisms of, and the effects that, environmental stimuli have on the magnitude and type of root exudation will ultimately improve our knowledge of processes determining soil CO2 emissions, ecosystem functioning and how to improve the sustainability of agricultural production.

  • Combination of techniques to quantify the distribution of bacteria in their soil microhabitats at different spatial scales

    Juyal A, Otten W, Falconer R, Hapca S, Schmidt H, Baveye PC, Eickhorst T
    2019 - Geoderma, 334: 165-174

    Abstract: 

    To address a number of issues of great societal concern at the moment, like the sequestration of carbon, information is direly needed about interactions between soil architecture and microbial dynamics. Unfortunately, soils are extremely complex, heterogeneous systems comprising highly variable and dynamic micro-habitats that have significant impacts on the growth and activity of inhabiting microbiota. Data remain scarce on the influence of soil physical parameters characterizing the pore space on the distribution and diversity of bacteria. In this context, the objective of the research described in this article was to develop a method where X-ray microtomography, to characterize the soil architecture, is combined with fluorescence microscopy to visualize and quantify bacterial distributions in resin-impregnated soil sections. The influence of pore geometry (at a resolution of 13.4 μm) on the distribution of Pseudomonas fluorescens was analysed at macro- (5.2 mm × 5.2 mm), meso- (1 mm × 1 mm) and microscales (0.2 mm × 0.2 mm) based on an experimental setup simulating different soil architectures. The cell density of P. fluorescenswas 5.59 x 107(SE 2.6 x 106) cells g−1 soil in 1–2 mm and 5.84 x 107(SE 2.4 x 106) cells g−1 in 2–4 mm size aggregates soil. Solid-pore interfaces influenced bacterial distribution at micro- and macroscale, whereas the effect of soil porosity on bacterial distribution varied according to three observation scales in different soil architectures. The influence of soil porosity on the distribution of bacteria in different soil architectures was observed mainly at the macroscale, relative to micro- and mesoscales. Experimental data suggest that the effect of pore geometry on the distribution of bacteria varied with the spatial scale, thus highlighting the need to consider an “appropriate spatial scale” to understand the factors that regulate the distribution of microbial communities in soils. The results obtained to date also indicate that the proposed method is a significant step towards a full mechanistic understanding of microbial dynamics in structured soils.

  • Coupled carbon and nitrogen losses in response to seven years of chronic warming in subarctic soils

    Marañon-Jimenez S, Peñuelas J, Richter A, Sigurdsson BD, Fuchslueger L, Leblans NIW, Janssens IA
    2019 - Soil Biology and Biochemistry, 134: 152-161

    Abstract: 

    Increasing temperatures may alter the stoichiometric demands of soil microbes and impair their capacity to stabilize carbon (C) and retain nitrogen (N), with critical consequences for the soil C and N storage at high latitude soils. Geothermally active areas in Iceland provided wide, continuous and stable gradients of soil temperatures to test this hypothesis. In order to characterize the stoichiometric demands of microbes from these subarctic soils, we incubated soils from ambient temperatures after the factorial addition of C, N and P substrates separately and in combination. In a second experiment, soils that had been exposed to different in situ warming intensities (+0, +0.5, +1.8, +3.4, +8.7, +15.9 °C above ambient) for seven years were incubated after the combined addition of C, N and P to evaluate the capacity of soil microbes to store and immobilize C and N at the different warming scenarios. The seven years of chronic soil warming triggered large and proportional soil C and N losses (4.1 ± 0.5% °C−1 of the stocks in unwarmed soils) from the upper 10 cm of soil, with a predominant depletion of the physically accessible organic substrates that were weakly sorbed in soil minerals up to 8.7 °C warming. Soil microbes met the increasing respiratory demands under conditions of low C accessibility at the expenses of a reduction of the standing biomass in warmer soils. This together with the strict microbial C:N stoichiometric demands also constrained their capacity of N retention, and increased the vulnerability of soil to N losses. Our findings suggest a strong control of microbial physiology and C:N stoichiometric needs on the retention of soil N and on the resilience of soil C stocks from high-latitudes to warming, particularly during periods of vegetation dormancy and low C inputs.

  • Vertical Redistribution of Soil Organic Carbon Pools After Twenty Years of Nitrogen Addition in Two Temperate Coniferous Forests

    Forstner, SJ, Wechselberger V, Müller S, Keiblinger KM, Díaz-Pinés E, Wanek W, Scheppi P, Hagedorn F, Gundersen P, Tatzber M, Gerzabek MH, Zechmeister-Boltenstern S
    2019 - Ecosystems, 22: 379-400

    Abstract: 

    Nitrogen (N) inputs from atmospheric deposition can increase soil organic carbon (SOC) storage in temperate and boreal forests, thereby mitigating the adverse effects of anthropogenic CO2 emissions on global climate. However, direct evidence of N-induced SOC sequestration from low-dose, long-term N addition experiments (that is, addition of < 50 kg N ha−1 y−1 for > 10 years) is scarce worldwide and virtually absent for European temperate forests. Here, we examine how tree growth, fine roots, physicochemical soil properties as well as pools of SOC and soil total N responded to 20 years of regular, low-dose N addition in two European coniferous forests in Switzerland and Denmark. At the Swiss site, the addition of 22 kg N ha−1 y−1 (or 1.3 times throughfall deposition) stimulated tree growth, but decreased soil pH and exchangeable calcium. At the Danish site, the addition of 35 kg N ha−1 y−1 (1.5 times throughfall deposition) impaired tree growth, increased fine root biomass and led to an accumulation of N in several belowground pools. At both sites, elevated N inputs increased SOC pools in the moderately decomposed organic horizons, but decreased them in the mineral topsoil. Hence, long-term N addition led to a vertical redistribution of SOC pools, whereas overall SOC storage within 30 cm depth was unaffected. Our results imply that an N-induced shift of SOC from older, mineral-associated pools to younger, unprotected pools might foster the vulnerability of SOC in temperate coniferous forest soils.

  • Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability

    Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, Zheng Q, Imai B, Prommer J, Weidinger M, Schweiger P, Eichorst SA, Wagner M, Richter A, Schintlmeister A, Woebken D, Kaiser C
    2019 - Frontiers Microbioly, 10: Article 168

    Abstract: 

    Plant roots release recent photosynthates into the rhizosphere, accelerating decomposition of organic matter by saprotrophic soil microbes (’rhizosphere priming effect’) which consequently increases nutrient availability for plants. However, about 90% of all higher plant species are mycorrhizal, transferring a significant fraction of their photosynthates directly to their fungal partners. Whether mycorrhizal fungi pass on plant-derived carbon (C) to bacteria in root-distant soil areas, i.e. incite a ‘hyphosphere priming effect’, is not known. Experimental evidence for C transfer from mycorrhizal hyphae to soil bacteria is limited, especially for ectomycorrhizal systems. As ectomycorrhizal fungi possess enzymatic capabilities to degrade organic matter themselves, it remains unclear whether they cooperate with soil bacteria by providing photosynthates, or compete for available nutrients.

    To investigate a possible C transfer from ectomycorrhizal hyphae to soil bacteria, and its response to changing nutrient availability, we planted young beech trees (Fagus sylvatica) into ‘split-root’ boxes, dividing their root systems into two disconnected soil compartments. Each of these compartments was separated from a litter compartment by a mesh penetrable for fungal hyphae, but not for roots. Plants were exposed to a 13C-CO2–labeled atmosphere, while 15N-labeled ammonium and amino acids were added to one side of the split-root system.

    We found a rapid transfer of recent photosynthates via ectomycorrhizal hyphae to bacteria in root-distant soil areas. Fungal and bacterial phospholipid fatty acid (PLFA) biomarkers were significantly enriched in hyphae-exclusive compartments 24 h after 13C-CO2–labeling. Isotope imaging with nanometer-scale secondary ion mass spectrometry (NanoSIMS) allowed for the first time in situ visualization of plant-derived C and N taken up by extraradical fungal hyphae, and in microbial cells thriving on hyphal surfaces. When N was added to the litter compartments, bacterial biomass and the amount of incorporated 13C strongly declined. Interestingly, this effect was also observed in adjacent soil compartments where added N was only available for bacteria through hyphal transport, indicating that ectomycorrhizal fungi were acting on soil bacteria. Together, our results demonstrate that (i) ectomycorrhizal hyphae rapidly transfer plant-derived C to bacterial communities in root-distant areas, and (ii) this transfer promptly responds to changing soil nutrient conditions.

  • Growth explains microbial carbon use efficiency across soils differing in land use and geology

    Zheng Q, Hu Y, zhang S, Noll L, Boeckle T, Richter A, Wanek W
    2019 - Soil Biology and Biochemistry, 128: 45-55

    Abstract: 

    The ratio of carbon (C) that is invested into microbial growth to organic C taken up is known as microbial carbon use efficiency (CUE), which is influenced by environmental factors such as soil temperature and soil moisture. How microbes will physiologically react to short-term environmental changes is not well understood, primarily due to methodological restrictions. Here we report on two independent laboratory experiments to explore short-term temperature and soil moisture effects on soil microbial physiology(i.e. respiration, growth, CUE, and microbial biomass turnover): (i) a temperature experiment with 1-day pre-incubation at 5, 15 and 25 °C at 60% water holding capacity (WHC), and (ii) a soil moisture/oxygen (O2) experiment with 7-day pre-incubation at 20 °C at 30%, 60% WHC (both at 21% O2) and 90% WHC at 1% O2. Experiments were conducted with soils from arable, pasture and forest sites derived from both silicate and limestone bedrocks. We found that microbial CUE responded heterogeneously though overall positively to short-term temperature changes, and decreased significantly under high moisture level (90% WHC)/suboxic conditions due to strong decreases in microbial growth. Microbial biomass turnover time decreased dramatically with increasing temperature, and increased significantly at high moisture level (90% WHC)/suboxic conditions. Our findings reveal that the responses of microbial CUE and microbial biomass turnover to short-term temperature and moisture/O2 changes depended mainly on microbial growth responses and less on respiration responses to the environmental cues, which were consistent across soils differing in land use and geology.

  • Wide-spread limitation of soil organic nitrogen transformations by substrate availability and not by extracellular enzyme content

    Noll L, zhang S, Zheng Q, Hu Y, Wanek W
    2019 - Soil Biology and Biochemistry, 133: 37-49

    Abstract: 

    Proteins constitute the single largest soil organic nitrogen (SON) reservoir and its decomposition drives terrestrial N availability. Protein cleavage by extracellular enzymes is the rate limiting step in the soil organic N cycle and can be controlled by extracellular enzyme production or protein availability/stabilization in soil. Both controls can be affected by geology and land use, as well as be vulnerable to changes in soil temperature and moisture/O2. To explore major controls of soil gross protein depolymerization we sampled six soils from two soil parent materials (calcareous and silicate), where each soil type included three land uses (cropland, pasture and forest). Soil samples were subjected to three temperature treatments (5, 15, 25 °C at 60% water-holding capacity (WHC) and aerobic conditions) or three soil moisture/O2 treatments (30 and 60% WHC at 21% O2, 90% WHC at 1% O2, at 20 °C) in short-term experiments. Samples were incubated for one day in the temperature experiment and for one week in the moisture/O2experiment. Gross protein depolymerization rates were measured by a novel 15N isotope pool dilution approach. The low temperature sensitivity of gross protein depolymerization, the lack of relationship with protease activity and strong effects of soil texture and pHdemonstrate that this process is constrained by organo-mineral associations and not by soil enzyme content. This also became apparent from the inverse effects in calcareous and silicate soils caused by water saturation/O2 limitation. We highlight that the specific soil mineralogy influenced the response of gross depolymerization rates to water saturation/O2 limitation, causing (I) increasing gross depolymerization rates due to release of adsorbed proteins by reductive dissolution of Fe- and Mn-oxyhydroxides in calcareous soils and (II) decreasing gross depolymerization rates due to mobilization of coagulating and toxic Al3+compounds in silicate soils.

  • Novel high-throughput approach to determine key processes of soil organic nitrogen cycling: Gross protein depolymerization and microbial amino acid uptake

    Noll L, zhang S, Wanek W
    2019 - Soil Biology and Biochemistry, 130: 73-81

    Abstract: 

    Proteins comprise the largest soil N reservoir but cannot be taken up directly by microorganisms and plants due to size constraints and stabilization of proteins in organo-mineral associations. Therefore the cleavage of this high molecular weight organic N to smaller soluble compounds as amino acids is a key step in the terrestrial N cycle. In the last years two isotope pool dilution approaches have been successfully established to measure gross rates of protein depolymerization and microbial amino acid uptake in soils. However, both require laborious sample preparation and analyses, which limits sample throughput. Therefore, we here present a novel isotope pool dilution approach based on the addition of 15N-labeled amino acids to soils and subsequent concentration and 15N analysis by the oxidation of α-amino groups to NO2 and further reduction to N2O, followed by purge-and-trap isotope ratio mass spectrometry (PT-IRMS). We applied this method in mesocosm experiments with forest and meadow soils as well as with a cropland soil amended with either organic C (cellulose) or organic N (bovine serum albumin). To measure direct organic N mineralization to NH4+, the latter was captured in acid traps and analyzed by an elemental analyzer coupled to an isotope ratio mass spectrometer (EA-IRMS). Our results demonstrate that the proposed method provides fast and precise measurements of at%15N even at low amino acid concentrations, allows high sample throughput and enables parallel estimations of instantaneous organic N mineralization rates.

  • Variation in rhizosphere priming and microbial growth and carbon use efficiency caused by wheat genotypes and temperatures

    Yin L, Corneo PE, Richter A, Wang P, Cheng W, Dijkstra FA
    2019 - Soil Biology and Biochemistry, 134: 54-61

    Abstract: 

    Living roots can influence microbial decomposition of soil organic matter, which has been referred to as the rhizosphere priming effect (RPE). Both microbial carbon efficiency (CUE) and microbial growth and turnover rates are associated with microbial decomposition and respiration of soil-derived C, but their linkage to the RPE remains poorly understood. Here we used a natural 13C tracer method to determine the RPE in soils planted with two wheat genotypes (249 or IAW2013) grown at high (30/24 °C during day/night) and low temperature (25/17 °C during day/night). We also determined microbial CUE, growth and biomassturnover rate using a substrate-independent H218O labeling method. The RPE varied from −2 to +455%, with significant effects of genotype, sampling date and their interaction with temperature. Compared to the unplanted control, microbial biomass C and growth/turnover rate were both enhanced in planted pots, with an average increase of 17% and 70%, respectively. Microbial CUE was lowest in pots planted with IAW2013 at low temperature, but there were no significant main effects of planting and temperature. Microbial biomass growth/turnover rate together with CUE accounted for 83% of the variation in soil-derived CO2, with a relatively larger contribution of microbial biomass growth/turnover rate (52%) than CUE (31%). Furthermore, using linear regression, we demonstrated that the RPE was significantly positively related to microbial biomass growth/turnover rate. No net soil organic C (SOC) loss or gain was detected, indicating that any increase in SOC due to increased microbial growth/turnover was counteracted by C loss caused by a higher RPE during the relatively short time of planting. These findings suggest that microbial biomass turnover associated with growth could control the loss of SOC with planting. We highlight the importance of plant-induced changes in microbial CUE and biomass growth/turnover for long-term soil C dynamics.

  • Low yield and abiotic origin of NO formed by the complete nitrifier Nitrospira inopinata

    Kits KD, Jung MY, Vierheilig J, Pjevac P, Sedlacek CJ, Liu S, Herbold C, Stein LY, Richter A, Wissel H, Brüggemann N, Wagner M, Daims H
    2019 - Nature Communications, 1: Article 1836

    Abstract: 

    Nitrous oxide (NO) and nitric oxide (NO) are atmospheric trace gases that contribute to climate change and affect stratospheric and ground-level ozone concentrations. Ammonia oxidizing bacteria (AOB) and archaea (AOA) are key players in the nitrogen cycle and major producers of NO and NO globally. However, nothing is known about NO and NO production by the recently discovered and widely distributed complete ammonia oxidizers (comammox). Here, we show that the comammox bacterium Nitrospira inopinata is sensitive to inhibition by an NO scavenger, cannot denitrify to NO, and emits NO at levels that are comparable to AOA but much lower than AOB. Furthermore, we demonstrate that NO formed by N. inopinata formed under varying oxygen regimes originates from abiotic conversion of hydroxylamine. Our findings indicate that comammox microbes may produce less NO during nitrification than AOB.

  • Widespread soil bacterium that oxidizes atmospheric methane

    Tveit AT, Hestnes AG, Robinson SL, Schintlmeister A, Dedysh SN, Jehmlich N, von Bergen M, Herbold CW, Wagner M, Richter A, Svenning MM
    2019 - Proceedings of the National Academy of Sciences of the United States of America (PNAS), 17: 8515-8524

    Abstract: 

    The global atmospheric level of methane (CH), the second most important greenhouse gas, is currently increasing by ∼10 million tons per year. Microbial oxidation in unsaturated soils is the only known biological process that removes CH from the atmosphere, but so far, bacteria that can grow on atmospheric CH have eluded all cultivation efforts. In this study, we have isolated a pure culture of a bacterium, strain MG08 that grows on air at atmospheric concentrations of CH [1.86 parts per million volume (p.p.m.v.)]. This organism, named , is globally distributed in soils and closely related to uncultured members of the upland soil cluster α. CH oxidation experiments and C-single cell isotope analyses demonstrated that it oxidizes atmospheric CH aerobically and assimilates carbon from both CH and CO Its estimated specific affinity for CH (a) is the highest for any cultivated methanotroph. However, growth on ambient air was also confirmed for and , close relatives with a lower specific affinity for CH, suggesting that the ability to utilize atmospheric CH for growth is more widespread than previously believed. The closed genome of MG08 encodes a single particulate methane monooxygenase, the serine cycle for assimilation of carbon from CH and CO, and CO fixation via the recently postulated reductive glycine pathway. It also fixes dinitrogen and expresses the genes for a high-affinity hydrogenase and carbon monoxide dehydrogenase, suggesting that atmospheric CH oxidizers harvest additional energy from oxidation of the atmospheric trace gases carbon monoxide (0.2 p.p.m.v.) and hydrogen (0.5 p.p.m.v.).

  • Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment

    Kitzinger K, Padilla CC, Marchant HK, Hach PF, Herbold CW, Kidane AT, Könneke M, Littmann S, Mooshammer M, Niggemann J, Petriv S, Richter A, Stewart FJ, Wagner M, Kuypers MMM, Bristow LA
    2019 - Nature Microbiology, 4: 234-243

    Abstract: 

    Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms1. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations2,3. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium4,5,6. Yet, it is unclear whether patterns observed in culture extend to marine Thaumarchaeota, and whether Thaumarchaeota in the ocean directly utilize urea and cyanate or rely on co-occurring microorganisms to break these substrates down to ammonium. Urea utilization has been reported for marine ammonia-oxidizing communities7,8,9,10, but no evidence of cyanate utilization exists for marine ammonia oxidizers. Here, we demonstrate that in the Gulf of Mexico, Thaumarchaeota use urea and cyanate both directly and indirectly as energy and N sources. We observed substantial and linear rates of nitrite production from urea and cyanate additions, which often persisted even when ammonium was added to micromolar concentrations. Furthermore, single-cell analysis revealed that the Thaumarchaeota incorporated ammonium-, urea- and cyanate-derived N at significantly higher rates than most other microorganisms. Yet, no cyanases were detected in thaumarchaeal genomic data from the Gulf of Mexico. Therefore, we tested cyanate utilization in Nitrosopumilus maritimus, which also lacks a canonical cyanase, and showed that cyanate was oxidized to nitrite. Our findings demonstrate that marine Thaumarchaeota can use urea and cyanate as both an energy and N source. On the basis of these results, we hypothesize that urea and cyanate are substrates for ammonia-oxidizing Thaumarchaeota throughout the ocean.

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